Abstract
BackgroundDigestive cells are present in all metazoans and provide the energy necessary for the whole organism. Pancreatic exocrine cells are a unique vertebrate cell type involved in extracellular digestion of a wide range of nutrients. Although the organization and regulation of this cell type is intensively studied in vertebrates, its evolutionary history is still unknown. In order to understand which are the elements that define the pancreatic exocrine phenotype, we have analyzed the expression of genes that contribute to specification and function of this cell-type in an early branching deuterostome, the sea urchin Strongylocentrotus purpuratus.ResultsWe defined the spatial and temporal expression of sea urchin orthologs of pancreatic exocrine genes and described a unique population of cells clustered in the upper stomach of the sea urchin embryo where exocrine markers are co-expressed. We used a combination of perturbation analysis, drug and feeding experiments and found that in these cells of the sea urchin embryo gene expression and gene regulatory interactions resemble that of bona fide pancreatic exocrine cells. We show that the sea urchin Ptf1a, a key transcriptional activator of digestive enzymes in pancreatic exocrine cells, can substitute for its vertebrate ortholog in activating downstream genes.ConclusionsCollectively, our study is the first to show with molecular tools that defining features of a vertebrate cell-type, the pancreatic exocrine cell, are shared by a non-vertebrate deuterostome. Our results indicate that the functional cell-type unit of the vertebrate pancreas may evolutionarily predate the emergence of the pancreas as a discrete organ. From an evolutionary perspective, these results encourage to further explore the homologs of other vertebrate cell-types in traditional or newly emerging deuterostome systems.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-016-0686-0) contains supplementary material, which is available to authorized users.
Highlights
Digestive cells are present in all metazoans and provide the energy necessary for the whole organism
We report that the components of the specification pathway and expression for zymogen genes are active in an early branching deuterostome, which suggests that the exocrine cell type may predate the evolution of the vertebrate pancreas
Characterization of regulatory and differentiation signatures for sea urchin pancreatic exocrine-like cells We identified sea urchin orthologs of regulatory genes with a known conserved role in pancreatic exocrine cell development
Summary
Digestive cells are present in all metazoans and provide the energy necessary for the whole organism. Pancreatic exocrine cells are a unique vertebrate cell type involved in extracellular digestion of a wide range of nutrients. Ptf1a has a double role, first in early pancreas specification, and later in acinar cell differentiation and maintenance [11–13], while Mist is necessary for full maturation of the acinar cell phenotype [14]. Notch appears to prevent pancreatic exocrine development, while FGF signaling mediates growth, morphogenesis and differentiation of exocrine cells [16–18]. In both mouse and zebrafish, Notch and its target genes inhibit the activity of the Ptf complex in the exocrine cells, and loss of Notch function results in accelerated development of exocrine pancreas [19]
Sign-in/Register to view highlights & summary Sign-in/Register to access full text options 
Talk to us
Join us for a 30 min session where you can share your feedback and ask us any queries you have
Schedule a callDisclaimer: All third-party content on this website/platform is and will remain the property of their respective owners and is provided on "as is" basis without any warranties, express or implied. Use of third-party content does not indicate any affiliation, sponsorship with or endorsement by them. Any references to third-party content is to identify the corresponding services and shall be considered fair use under The CopyrightLaw.
